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Originally published In Press as doi:10.1074/jbc.M006399200 on September 25, 2000

J. Biol. Chem., Vol. 275, Issue 51, 40357-40364, December 22, 2000
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Structural Requirements for the Adherence of Plasmodium falciparum-infected Erythrocytes to Chondroitin Sulfate Proteoglycans of Human Placenta*

Abdulnaser AlkhalilDagger , Rajeshwara N. AchurDagger , Manojkumar ValiyaveettilDagger , Christian F. Ockenhouse§, and D. Channe GowdaDagger

From the Dagger  Department of Biochemistry and Molecular Biology, Georgetown University Medical Center, Washington, D. C. 20007 and the § Department of Immunology, Walter Reed Army Institute of Research, Silver Spring, Maryland 20910

Plasmodium falciparum infection during pregnancy results in the accumulation of infected red blood cells (IRBCs) in the placenta, leading to poor pregnancy outcome. In the preceding paper (Achur, R.N., Valiyaveettil, M., Alkhalil, A., Ockenhouse, C. F., and Gowda, D.C. (2000) J. Biol. Chem. 275, 40344-40356), we reported that unusually low sulfated chondroitin sulfate proteoglycans (CSPGs) in the intervillous spaces of the placenta mediate the IRBC adherence. In this study, we report the structural requirements for the adherence and the minimum chondroitin 4-sulfate (C4S) structural motif that supports IRBC adherence. Partially sulfated C4Ss with varying sulfate contents were prepared by solvolytic desulfation of a fully sulfated C4S. These and other nonmodified C4Ss, with different proportions of 4-, 6-, and nonsulfated disaccharide repeats, were analyzed for inhibition of IRBC adherence to the placental CSPG. C4Ss containing 30-50% 4-sulfated and 50-70% nonsulfated disaccharide repeats efficiently inhibited IRBC adherence; C6S had no inhibitory activity. Oligosaccharides of varying sizes were prepared by the partial depolymerization of C4Ss containing varying levels of 4-sulfation, and their ability to inhibit the IRBC adherence was studied. Oligosaccharides with six or more disaccharide repeats inhibited IRBC adherence to the same level as that of the intact C4Ss, indicating that a dodecasaccharide is the minimum structural motif required for optimal IRBC adherence. Of the C4S dodecasaccharides, only those with two or three sulfate groups per molecule showed maximum IRBC inhibition. These data define the structural requirements for the IRBC adherence to placental CSPGs with implications for the development of therapeutics for maternal malaria.

* This work was supported by grants from the Burroughs Wellcome Fund for New Initiatives in Malaria Research and by Grant AI45086 from NIAID, National Institutes of Health.The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

To whom correspondence should be addressed: Dept. of Biochemistry and Molecular Biology, Georgetown University Medical Center, 3900 Reservoir Rd., N.W., Washington, DC 20007. Tel.: 202-687-3840; Fax: 202-687-7186; E-mail: gowda@bc.georgetown.edu.

Copyright © 2000 by The American Society for Biochemistry and Molecular Biology, Inc.
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